Abstract

In mammalian peripheral nerves, unmyelinated C-fibers usually outnumber myelinated A-fibers. By using transmission electron microscopy, we recently showed that the saphenous nerve of the naked mole-rat (Heterocephalus glaber) has a C-fiber deficit manifested as a substantially lower C:A-fiber ratio compared with other mammals. Here we determined the uniqueness of this C-fiber deficit by performing a quantitative anatomical analysis of several peripheral nerves in five further members of the Bathyergidae mole-rat family: silvery (Heliophobius argenteocinereus), giant (Fukomys mechowii), Damaraland (Fukomys damarensis), Mashona (Fukomys darlingi), and Natal (Cryptomys hottentotus natalensis) mole-rats. In the largely cutaneous saphenous and sural nerves, the naked mole-rat had the lowest C:A-fiber ratio (∼1.5:1 compared with ∼3:1), whereas, in nerves innervating both skin and muscle (common peroneal and tibial) or just muscle (lateral/medial gastrocnemius), this pattern was mostly absent. We asked whether lack of hair follicles alone accounts for the C-fiber paucity by using as a model a mouse that loses virtually all its hair as a consequence of conditional deletion of the β-catenin gene in the skin. These β-catenin loss-of function mice (β-cat LOF mice) displayed only a mild decrease in C:A-fiber ratio compared with wild-type mice (4.42 compared with 3.81). We suggest that the selective cutaneous C-fiber deficit in the cutaneous nerves of naked mole-rats is unlikely to be due primarily to lack of skin hair follicles. Possible mechanisms contributing to this unique peripheral nerve anatomy are discussed. J. Comp. Neurol. 520:2785–2803, 2012. © 2012 Wiley Periodicals, Inc.

Highlights

  • The axons present in the peripheral nerves of mammals can originate from motor neurons, pre- and postganglionic autonomic neurons, and sensory neurons with their cell bodies in the trigeminal and dorsal root ganglia

  • The sural nerve, which contains predominantly cutaneous axons and innervates the lateral calf and foot (Peyronnard and Charron, 1982; Lewin and McMahon, 1991a,b), has been observed to contain a C:A-fiber ratio of $4:1 in both humans and rabbits, Oryctolagus cuniculus (Ochoa and Mair, 1969; Schwab et al, 1984). In contrast to this generally conserved high C:A-fiber ratio, we recently found that the saphenous nerve in African naked-mole rats (Heterocephalus glaber) has a pronounced deficit in C-fibers, so that the C:A-fiber ratio is only $1.1:1 (Park et al, 2008)

  • We first set out to determine whether the very low C:Afiber ratio that we had previously observed in the largely cutaneous saphenous nerve of the naked mole-rat (Park et al, 2008) is consistent in nerves that innervate other targets in this species and how A- and C-fiber counts compare across bathyergids

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Summary

Introduction

The axons present in the peripheral nerves of mammals can originate from motor neurons, pre- and postganglionic autonomic neurons, and sensory neurons with their cell bodies in the trigeminal and dorsal root ganglia. The need to detect potentially damaging stimuli has been the selection pressure behind the evolution of nociceptors, and their importance for protective reflexes may explain the fact that C-fibers often outnumber A-fibers (Smith and Lewin, 2009). This predominance of C-fibers over A-fibers is well documented for the saphenous nerve, which normally contains only cutaneous afferents innervating the medial knee, lower leg, and foot (Zimmermann et al, 2009). The sural nerve, which contains predominantly cutaneous axons and innervates the lateral calf and foot (Peyronnard and Charron, 1982; Lewin and McMahon, 1991a,b), has been observed to contain a C:A-fiber ratio of $4:1 in both humans and rabbits, Oryctolagus cuniculus (Ochoa and Mair, 1969; Schwab et al, 1984)

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